The evolutionary history of the HUP domain. (2nd January 2022)

• Record Type: Journal Article
• Authors: Gruic-Sovulj, Ita; Longo, Liam M.; Jabłońska, Jagoda; Tawfik, Dan S.
• Is Part Of: Critical reviews in biochemistry and molecular biology. Volume 57:Number 1(2022)
• Page Start: 1
• Page End: 15
• Publication Date: 2022-01-02
• Subjects: HIGH motif -- PP-ATPase -- aminoacyl-tRNA synthetases -- Rossmannoid -- nucleotide binding domain -- protein evolution -- last universal common ancestor; Biochemistry -- Periodicals; Molecular biology -- Periodicals; Biochemistry -- Periodicals; Molecular Biology -- Periodicals; Review Literature -- Periodicals; 572
• DOI: 10.1080/10409238.2021.1957764
• Languages: English
• ISSNs: 1040-9238

Abstract

Abstract: Among the enzyme lineages that undoubtedly emerged prior to the last universal common ancestor is the so-called HUP, which includes Class I aminoacyl tRNA synthetases (AARSs) as well as enzymes mediating NAD, FAD, and CoA biosynthesis. Here, we provide a detailed analysis of HUP evolution, from emergence to structural and functional diversification. The HUP is a nucleotide binding domain that uniquely catalyzes adenylation via the release of pyrophosphate. In contrast to other ancient nucleotide binding domains with the αβα sandwich architecture, such as P-loop NTPases, the HUP's most conserved feature is not phosphate binding, but rather ribose binding by backbone interactions to the tips of β1 and/or β4. Indeed, the HUP exhibits unusual evolutionary plasticity and, while ribose binding is conserved, the location and mode of binding to the base and phosphate moieties of the nucleotide, and to the substrate(s) reacting with it, have diverged with time, foremost along the emergence of the AARSs. The HUP also beautifully demonstrates how a well-packed scaffold combined with evolvable surface elements promotes evolutionary innovation. Finally, we offer a scenario for the emergence of the HUP from a seed βαβ fragment, and suggest that despite an identical architecture, the HUP and the Rossmann represent independent emergences.