Cold-Adaptation Signatures in the Ligand Rebinding Kinetics to the Truncated Hemoglobin of the Antarctic Bacterium Pseudoalteromonas haloplanktis TAC125
Authors: Boubeta F.M.; Boechi L.; Estrin D.; Patrizi B.; Di Donato M.; Iagatti A.; Giordano D.; Verde C.; Bruno S.; Abbruzzetti S.; Viappiani C.
Autors Affiliation: Consejo Nacl Invest Cient & Tecn, Inst Quim Fis Mat Medio Ambiente & Energia INQUIM, C1428EHA, Buenos Aires, DF, Argentina; Univ Buenos Aires, C1428EHA, Buenos Aires, DF, Argentina; Univ Buenos Aires, Fac Ciencias Exactas & Nat, Inst Calculo, C1428EGA, Buenos Aires, DF, Argentina; Univ Firenze, European Lab Non Linear Spect LENS, Via Nello Carrara 1, I-50019 Florence, Italy; CNR, INO, Largo Fermi 6, I-50125 Florence, Italy; CNR, Inst Biosci & BioResources IBBR, Via Pietro Castellino 111, I-80131 Naples, Italy; Stn Zool Anton Dohrn, I-80121 Naples, Italy; Univ Parma, Dipartimento Sci Alimenti & Farmaco, Parco Area Sci 23A, I-43124 Parma, Italy; Univ Parma, Dipartimento Sci Matemat Fis & Informat, Parco Area Sci 7A, I-43124 Parma, Italy
Abstract: Cold-adapted organisms have evolved proteins endowed with higher flexibility and lower stability in comparison to their thermophilic homologues, resulting in enhanced reaction rates at low temperatures. In this context, protein-bound water molecules were suggested to play a major role, and their weaker interactions at protein active sites have been associated with cold adaptation. In this work, we tested this hypothesis on truncated hemoglobins (a family of microbial heme-proteins of yet-unclear function) applying molecular dynamics simulations and ligand-rebinding kinetics on a protein from the Antarctic bacterium Pseudoalteromonas haloplanktis TAC125 in comparison with its thermophilic Thermobifida fusca homologue. The CO rebinding kinetics of the former highlight several geminate phases, with an unusually long-lived geminate intermediate. An articulated tunnel with at least two distinct docking sites was identified by analysis of molecular dynamics simulations and was suggested to be at the origin of the unusual geminate rebinding phase. Water molecules are present in the distal pocket, but their stabilization by TrpG8, TyrB10, and HisCD1 is much weaker than in thermophilic Thermobifida fusca truncated hemoglobin, resulting in a faster geminate rebinding. Our results support the hypothesis that weaker water-molecule interactions at the reaction site are associated with cold adaptation.
Journal/Review: JOURNAL OF PHYSICAL CHEMISTRY B
Volume: 122 (49) Pages from: 11649 to: 11661
More Information: This study was carried out in the framework of the SCAR program “Antarctic Thresholds: Ecosystem Resilience and Adaptation” (AnT-ERA). C.V., D.G., and S.B. acknowledge financial support by the Italian National Programme (PdR 2013/AZ1.20) for Antarctic Research (PNRA). D.E. and L.B. acknowledge funding from Universidad de Buenos Aires (Grant UBACYT 20020130100097BA) and Agencia Nacional de Promocion Cientifica y Tecnologica Grants PICT 2014-1022, PICT 2015-2761, and 2015-2989. L.B. acknowledges Bunge & Born Foundation for financial support. S.A. and C.V. acknowledge Azienda USL di Piacenza and Fondazione di Piacenza e Vigevano for financial support. C.V. acknowledges S. E. Braslavsky for the kind donation of the Spectron laser. All computer simulations were run at Centro de Computo de Alto Rendimiento (CECAR). This project has received funding from the European Union’s Horizon 2020 Research and Innovation Programme under Grant 654148 Laserlab-Europe (Laserlab-Europe, H2020 EC-GA 654148).KeyWords: Bacteria; Hemoglobin; Kinetics; Ligands; Molecular dynamics; Molecules; Reaction rates, Antarctic bacteria; Bound water molecules; Geminate rebinding; Ligand rebinding; Molecular dynamics simulations; Pseudoalteromonas haloplanktis; Thermobifida fusca; Truncated hemoglobins, ProteinsDOI: 10.1021/acs.jpcb.8b07682Citations: 4data from “WEB OF SCIENCE” (of Thomson Reuters) are update at: 2020-08-02References taken from IsiWeb of Knowledge: (subscribers only)Connecting to view paper tab on IsiWeb: Click hereConnecting to view citations from IsiWeb: Click here