Identification of Evolutionarily Conserved Nuclear Matrix Proteins and Their Prokaryotic Origins

Abstract

Compared to prokaryotic cells, a typical eukaryotic cell is much more complex along with its endomembrane system and membrane-bound organelles. Although the endosymbiosis theories convincingly explain the evolution of membrane-bound organelles such as mitochondria and chloroplasts, very little is understood about the evolutionary origins of the nucleus, the defining feature of eukaryotes. Most studies on nuclear evolution have not been able to take into consideration the underlying structural framework of the nucleus, attributed to the nuclear matrix (NuMat), a ribonucleoproteinaceous structure. This can largely be attributed to the lack of annotation of its core components. Since NuMat has been shown to provide a structural platform for facilitating a variety of nuclear functions such as replication, transcription, and splicing, it is important to identify its protein components to better understand these processes. In this study, we address this issue using the developing embryos of Drosophila melanogaster and Danio rerio and identify 362 core NuMat proteins that are conserved between the two organisms. We further compare our results with publicly available Mus musculus NuMat dataset and Homo sapiens cellular localization dataset to define the core homologous NuMat proteins consisting of 252 proteins. We find that of them, 86 protein groups have originated from preexisting proteins in prokaryotes. While 36 were conserved across all eukaryotic supergroups, 14 new proteins evolved before the evolution of the last eukaryotic common ancestor and together, these 50 proteins out of the 252 core conserved NuMat proteins are conserved across all eukaryotes, indicating their indispensable nature for nuclear function for over 1.5 billion years of eukaryotic history. Our analysis paves the way to understand the evolution of the complex internal nuclear architecture and its functions.

True-to-scale DNA-density maps correlate with major accessibility differences between active and inactive chromatin

“…The nuclear matrix proteome 55 may form phase-separated droplets within the IC with the help of non-coding RNA sequences 56, 57 . Like assembled macromolecular machineries, such condensates are excluded by size from the INC and may serve as storage vesicles for the formation of functional machineries.…”

“…Recent evidence has suggested a dual nature of chromatin (Hansen et al, 2021; Strickfaden et al, 2020). The nuclear matrix proteome (Sureka and Mishra, 2021) may form phase-separated droplets within the IC with the help of non-coding RNA sequences (Farabella et al, 2021; Razin and Gavrilov, 2021). Like assembled macromolecular machineries, such condensates are excluded by size from the INC and may serve as storage vesicles for the formation of functional machineries.…”

Cultured deep-sea PVC bacteria shed light on eukaryogenesis

“…S1C, panel 4). Although the presence of the nucleus and other membrane-bound organelles are hallmark features of eukaryotic cells, a recent cross-species proteomic analysis of the prokaryote nuclear matrix structure identified a significant fraction of such proteins evolutionary related to counterparts in eukaryotes 14 . In line with emerging studies highlighting unique properties of PCV bacteria 12 , we conclude that PVC strains are differentiated from how bacteria are conventionally defined by their abundant eukaryotic signatures as well as a high structural complexity.…”

Biochemical deconstruction and reconstruction of Nuclear Matrix reveals the layers of nuclear organization

“…CC-BY-NC-ND 4.0 International license available under a (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. The protocol for the preparation of NuMat has previously been described in (Sureka and Mishra, 2021) and used here with minor modifications, described as follows.…”