Inhibitory to non-inhibitory evolution of the ζ subunit of the F1FO-ATPase of Paracoccus denitrificans and α-proteobacteria as related to mitochondrial endosymbiosis

Frontiers in Molecular Biosciences

Molecular Biosciences

Miguel Ángel Cevallos¹  Raquel Ortega²  Oliver Sotelo-Serrano²  Gilberto Garduño-Javier²  Emiliano Salinas-López²  Jorge Brito-Sánchez²  José J. García-Trejo²  Francisco Mendoza-Hoffmann³  Leticia Ramírez-Silva⁴  Gerardo Pérez-Hernández⁵  Salvador Uribe-Carvajal⁶  Cristina Uribe-Álvarez⁶  Heliodoro Celis-Sandoval⁶  Damiano Buratto⁷  Lingyun Yang⁸ 

[1] Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México (U.N.A.M.), Ciudad de México, México;Departamento de Biología, Facultad de Química, Ciudad Universitaria, Universidad Nacional Autónoma de México (U.N.A.M.), Ciudad de México, México;Departamento de Biología, Facultad de Química, Ciudad Universitaria, Universidad Nacional Autónoma de México (U.N.A.M.), Ciudad de México, México;iHuman Institute, ShanghaiTech University, Shanghai, China;Departamento de Bioquímica, Facultad de Medicina, Universidad Nacional Autónoma de México (U.N.A.M.), Ciudad de México, México;Departamento de Ciencias Naturales, Universidad Autónoma Metropolitana, Unidad Cuajimalpa, Ciudad de México, México;Instituto de Fisiología Celular, Universidad Nacional Autónoma de México (U.N.A.M.), Ciudad de México, México;Shanghai Institute for Advanced Immunochemical Studies, ShanghaiTech University, Shanghai, China;iHuman Institute, ShanghaiTech University, Shanghai, China;

关键词: evolution;    ATP synthase;    α-proteobacteria;    mitochondria;    endosymbiosis;    zeta subunit;    ζ;    Paracoccus denitrificans;   

DOI  :  10.3389/fmolb.2023.1184200

 received in 2023-03-11, accepted in 2023-08-01,  发布年份 2023

来源: Frontiers

【 摘 要 】

Introduction: The ζ subunit is a potent inhibitor of the F1FO-ATPase of Paracoccus denitrificans (PdF1FO-ATPase) and related α-proteobacteria different from the other two canonical inhibitors of bacterial (ε) and mitochondrial (IF1) F1FO-ATPases. ζ mimics mitochondrial IF1 in its inhibitory N-terminus, blocking the PdF1FO-ATPase activity as a unidirectional pawl-ratchet and allowing the PdF1FO-ATP synthase turnover. ζ is essential for the respiratory growth of P. denitrificans, as we showed by a Δζ knockout. Given the vital role of ζ in the physiology of P. denitrificans, here, we assessed the evolution of ζ across the α-proteobacteria class.Methods: Through bioinformatic, biochemical, molecular biology, functional, and structural analyses of several ζ subunits, we confirmed the conservation of the inhibitory N-terminus of ζ and its divergence toward its C-terminus. We reconstituted homologously or heterologously the recombinant ζ subunits from several α-proteobacteria into the respective F-ATPases, including free-living photosynthetic, facultative symbiont, and intracellular facultative or obligate parasitic α-proteobacteria.Results and discussion: The results show that ζ evolved, preserving its inhibitory function in free-living α-proteobacteria exposed to broad environmental changes that could compromise the cellular ATP pools. However, the ζ inhibitory function was diminished or lost in some symbiotic α-proteobacteria where ζ is non-essential given the possible exchange of nutrients and ATP from hosts. Accordingly, the ζ gene is absent in some strictly parasitic pathogenic Rickettsiales, which may obtain ATP from the parasitized hosts. We also resolved the NMR structure of the ζ subunit of Sinorhizobium meliloti (Sm-ζ) and compared it with its structure modeled in AlphaFold. We found a transition from a compact ordered non-inhibitory conformation into an extended α-helical inhibitory N-terminus conformation, thus explaining why the Sm-ζ cannot exert homologous inhibition. However, it is still able to inhibit the PdF1FO-ATPase heterologously. Together with the loss of the inhibitory function of α-proteobacterial ε, the data confirm that the primary inhibitory function of the α-proteobacterial F1FO-ATPase was transferred from ε to ζ and that ζ, ε, and IF1 evolved by convergent evolution. Some key evolutionary implications on the endosymbiotic origin of mitochondria, as most likely derived from α-proteobacteria, are also discussed.

【 授权许可】

Unknown   
Copyright © 2023 Mendoza-Hoffmann, Yang, Buratto, Brito-Sánchez, Garduño-Javier, Salinas-López, Uribe-Álvarez, Ortega, Sotelo-Serrano, Cevallos, Ramírez-Silva, Uribe-Carvajal, Pérez-Hernández, Celis-Sandoval and García-Trejo.