Lessons from the deep: mechanisms behind diversification of eukaryotic protein complexes

Prokopchuk, Galina; Butenko, Anzhelika; Dacks, Joel B.; Speijer, Dave; Field, Mark C.; Lukeš, Julius

doi:10.1111/brv.12988

Cited by 10 publications

(8 citation statements)

References 243 publications

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“…2). Instead, we propose that the sparse distribution likely arises from ongoing and repeated gene loss, as has been previously documented for other gene families across the Tree of Life [22,[24][25][26].…”

Section: Discussionmentioning

confidence: 61%

“…1B). We believe this pattern reflects a pattern of ongoing, repeated gene losses across eukaryotes, as has been found for other innate immune proteins [21][22][23] and other types of gene families surveyed across eukaryotes [22,[24][25][26]. We found that BUSCO completeness scores and data type (genomes vs. transcriptomes) were insufficient to explain the pattern of gene loss (Supp.…”

Section: Discovering Immune Homologs Across the Eukaryotic Tree Of Lifementioning

confidence: 60%

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Eukaryotic antiviral immune proteins arose via convergence, horizontal transfer, and ancient inheritance

Culbertson

Levin

2023

Preprint

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Animals use a variety of cell-autonomous innate immune proteins to detect viral infections and prevent replication. Recent studies have discovered that a subset of mammalian antiviral proteins have homology to anti-phage defense proteins in bacteria, implying that there are aspects of innate immunity that are shared across the Tree of Life. While the majority of these studies have focused on characterizing the diversity and biochemical functions of the bacterial proteins, the evolutionary relationships between animal and bacterial proteins are less clear. This ambiguity is partly due to the long evolutionary distances separating animal and bacterial proteins, which obscures their relationships. Here, we tackle this problem for three innate immune families (CD-NTases [including cGAS], STINGs, and Viperins) by deeply sampling protein diversity across eukaryotes. We find that Viperins are truly ancient immune proteins, likely inherited since the last eukaryotic common ancestor and possibly longer. In contrast, we find other immune proteins that arose via at least five independent events of horizontal gene transfer (HGT) from bacteria. Two of these events allowed algae to acquire new bacterial viperins, while three more HGT events gave rise to distinct superfamilies of eukaryotic CD-NTases: the OAS superfamily, which is widespread across eukaryotes; the Mab21 superfamily (containing cGAS) which has diversified via a series of animal-specific duplications, and a previously undefined eSMODS superfamily, which more closely resembles bacterial CD-NTases. Finally, we found that cGAS and STING proteins have substantially different histories, with STINGs arising via convergent domain shuffling in bacteria and eukaryotes. Overall, our findings paint a picture of eukaryotic innate immunity as highly dynamic, where eukaryotes build upon their ancient antiviral repertoires through the reuse of protein domains and by repeatedly sampling a rich reservoir of bacterial anti-phage genes.

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Section: Discussionmentioning

confidence: 61%

Section: Discovering Immune Homologs Across the Eukaryotic Tree Of Lifementioning

confidence: 60%

Eukaryotic antiviral immune proteins arose via convergence, horizontal transfer, and ancient inheritance

Culbertson

Levin

2023

Preprint

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“…Interestingly, in this case occasional gene loss might open up space for a duplicated gene to step in. [ 83 ] Duplications also allow more optimal “gene sharing,” for example, letting a metabolic enzyme become an eye lens crystallin. [ 84 ] Reconstructed gene trees might thus come up with ancient ancestral forms of diverged proteins, helping us understand how certain structures and functions evolved, even in the case of proteins now having completely different functions.…”

Section: Broader Applicability Of the Concept Of Trees Growing By Des...mentioning

confidence: 99%

The contours of evolution: In defence of Darwin's tree of life paradigm

van der Gulik,

Hoff,

Speijer

2024

BioEssays

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Both the concept of a Darwinian tree of life (TOL) and the possibility of its accurate reconstruction have been much criticized. Criticisms mostly revolve around the extensive occurrence of lateral gene transfer (LGT), instances of uptake of complete organisms to become organelles (with the associated subsequent gene transfer to the nucleus), as well as the implications of more subtle aspects of the biological species concept. Here we argue that none of these criticisms are sufficient to abandon the valuable TOL concept and the biological realities it captures. Especially important is the need to conceptually distinguish between organismal trees and gene trees, which necessitates incorporating insights into widely occurring LGT into modern evolutionary theory. We demonstrate that all criticisms, while based on important new findings, do not invalidate the TOL. After considering the implications of these new insights, we find that the contours of evolution are best represented by a TOL.

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“…found for other innate immune proteins [27][28][29] and other types of gene families surveyed across eukaryotes [28,[30][31][32]. Indeed, many of the species that lacked any of the immune homologs were represented by high-quality datasets (Ex: Metazoa, Chlorplastida, and Fungi).…”

Section: Plos Biologymentioning

confidence: 99%

Eukaryotic CD-NTase, STING, and viperin proteins evolved via domain shuffling, horizontal transfer, and ancient inheritance from prokaryotes

Culbertson,

Levin

2023

PLoS Biol

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Animals use a variety of cell-autonomous innate immune proteins to detect viral infections and prevent replication. Recent studies have discovered that a subset of mammalian antiviral proteins have homology to antiphage defense proteins in bacteria, implying that there are aspects of innate immunity that are shared across the Tree of Life. While the majority of these studies have focused on characterizing the diversity and biochemical functions of the bacterial proteins, the evolutionary relationships between animal and bacterial proteins are less clear. This ambiguity is partly due to the long evolutionary distances separating animal and bacterial proteins, which obscures their relationships. Here, we tackle this problem for 3 innate immune families (CD-NTases [including cGAS], STINGs, and viperins) by deeply sampling protein diversity across eukaryotes. We find that viperins and OAS family CD-NTases are ancient immune proteins, likely inherited since the earliest eukaryotes first arose. In contrast, we find other immune proteins that were acquired via at least 4 independent events of horizontal gene transfer (HGT) from bacteria. Two of these events allowed algae to acquire new bacterial viperins, while 2 more HGT events gave rise to distinct superfamilies of eukaryotic CD-NTases: the cGLR superfamily (containing cGAS) that has since diversified via a series of animal-specific duplications and a previously undefined eSMODS superfamily, which more closely resembles bacterial CD-NTases. Finally, we found that cGAS and STING proteins have substantially different histories, with STING protein domains undergoing convergent domain shuffling in bacteria and eukaryotes. Overall, our findings paint a picture of eukaryotic innate immunity as highly dynamic, where eukaryotes build upon their ancient antiviral repertoires through the reuse of protein domains and by repeatedly sampling a rich reservoir of bacterial antiphage genes.

show abstract

Lessons from the deep: mechanisms behind diversification of eukaryotic protein complexes

Cited by 10 publications

References 243 publications

Eukaryotic antiviral immune proteins arose via convergence, horizontal transfer, and ancient inheritance

Eukaryotic antiviral immune proteins arose via convergence, horizontal transfer, and ancient inheritance

The contours of evolution: In defence of Darwin's tree of life paradigm

Eukaryotic CD-NTase, STING, and viperin proteins evolved via domain shuffling, horizontal transfer, and ancient inheritance from prokaryotes

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