Ubiquitin fusion proteins in algae: implications for cell biology and the spread of photosynthesis

Abstract

BackgroundThe process of gene fusion involves the formation of a single chimeric gene from multiple complete or partial gene sequences. Gene fusion is recognized as an important mechanism by which genes and their protein products can evolve new functions. The presence-absence of gene fusions can also be useful characters for inferring evolutionary relationships between organisms.ResultsHere we show that the nuclear genomes of two unrelated single-celled algae, the cryptophyte Guillardia theta and the chlorarachniophyte Bigelowiella natans, possess an unexpected diversity of genes for ubiquitin fusion proteins, including novel arrangements in which ubiquitin occupies amino-terminal, carboxyl-terminal, and internal positions relative to its fusion partners. We explore the evolution of the ubiquitin multigene family in both genomes, and show that both algae possess a gene encoding an ubiquitin-nickel superoxide dismutase fusion protein (Ubiq-NiSOD) that is widely but patchily distributed across the eukaryotic tree of life – almost exclusively in phototrophs.ConclusionOur results suggest that ubiquitin fusion proteins are more common than currently appreciated; because of its small size, the ubiquitin coding region can go undetected when gene predictions are carried out in an automated fashion. The punctate distribution of the Ubiq-NiSOD fusion across the eukaryotic tree could serve as a beacon for the spread of plastids from eukaryote to eukaryote by secondary and/or tertiary endosymbiosis.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-5412-4) contains supplementary material, which is available to authorized users.

Ubiquitin and Ubiquitin-Like Proteins and Domains in Ribosome Production and Function: Chance or Necessity?

“…Only rarely, Ub is fused to other proteins in different architectures ( Table S2 ), although these arrangements are widely represented in the eukaryotic groups of animals, fungi, and plants ( Figure 3 ). In this sense, in a small group of mixotrophic algae, it has been reported that one or several N-terminal Ub moieties are fused in-frame inter alia to ribosomal protein P1, actin, a zinc-finger protein, a nickel superoxide dismutase, or a protein with similarity to bacterial integral membrane proteins [ 35 , 36 ]. A more careful study indicates that the Ub fusion to the latter three proteins is found in other eukaryotes, such as different types of algae and diverse fungi [ 36 ].…”

“…In this sense, in a small group of mixotrophic algae, it has been reported that one or several N-terminal Ub moieties are fused in-frame inter alia to ribosomal protein P1, actin, a zinc-finger protein, a nickel superoxide dismutase, or a protein with similarity to bacterial integral membrane proteins [ 35 , 36 ]. A more careful study indicates that the Ub fusion to the latter three proteins is found in other eukaryotes, such as different types of algae and diverse fungi [ 36 ]. Indeed, our analysis shows that the zf-AN1 (PF01428) and zf-RRN7 (PF11781) domains, which correspond to zinc-finger domains, are the most abundant ones in these unusual architectures (ca.…”

Ribosome heterogeneity in stem cells and development

“…In both humans and mice, there are four genes encoding ubiquitin: UBB and UBC encoding polyubiquitin precursor with ubiquitin repeats and RPS27A/eS31 and UBA52 encoding ubiquitin as in-frame fusions to RPS27A/eS31 and RPL40/eL40, respectively ( Park and Ryu, 2014 ). These RP-ubiquitin fusions (ubiquitin-S27A/L40) are identified across the full breadth of eukaryotic diversity ( Sibbald et al, 2019 ). Ubiquitin can be posttranslationally cleaved from RP–ubiquitin fusions.…”

The Ubiquitin Moiety of Ubi1 Is Required for Productive Expression of Ribosomal Protein eL40 in Saccharomyces cerevisiae

“…For both classes, free de novo ubiquitin is synthesized by proteolytic maturation from the corresponding precursor proteins. Only rarely, ubiquitin is encoded by monoubiquitin genes, as occurs in the protozoa Giardia lamblia and Entamoeba histolytica , or in algae as Guillardia theta and Bigelowiella natans [11,12,13].…”