New Lineage of Microbial Predators Adds Complexity to Reconstructing the Evolutionary Origin of Animals

Tikhonenkov, Denis V.; Mikhailov, Kirill V.; Hehenberger, Elisabeth; Karpov, Sergey A.; Prokina, Kristina; Esaulov, Anton S.; Belyakova, Olga I.; Mazei, Yuri A.; Mylnikov, Alexander P.; Aleoshin, Vladimir V.; Keeling, Patrick J.

doi:10.1016/j.cub.2020.08.061

Cited by 38 publications

(56 citation statements)

References 77 publications

(105 reference statements)

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“…A similar case concerns the unresolved position of the recently discovered Tunicaraptor unikontum, another predatory flagellate closely related to animals [84]. Depending on the taxon sampling used, T. unikontum may be sister to filastereans, Filozoa (which includes the filasterean-choanoflagellate-animal group), or it may be the earliest branching holozoan lineage [84]. Environmental surveys have also identified other putative new species falling within or related to different unicellular holozoan clades and even a potential novel lineage [85][86][87][88][89][90][91][92][93].…”

Section: Phylogenetic Framework Of Animals and Their Unicellular Relativesmentioning

confidence: 99%

“…Besides analyses of their genomes, comparisons of unicellular holozoans' biological traits can also provide a comprehensive reconstruction of the cellular foundations of the last unicellular ancestor of animals. In recent years, the lifestyles and cell biology of several unicellular holozoan species have been characterized at the transcriptomic and morphological level [24][25][26]42,45,51,70,84,[96][97][98][99][175][176][177][178][179][180]. Strikingly, each unicellular holozoan lineage features unique and distinctive traits that have changed our understanding of the biological nature of the last unicellular ancestor of animals.…”

Section: Reconstruction Of the Biological Features Of The Last Unicellular Ancestor Of Animals And Last Common Ancestor Of Animals 221 Pomentioning

confidence: 99%

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The origin of animals: an ancestral reconstruction of the unicellular-to-multicellular transition

et al. 2021

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How animals evolved from a single-celled ancestor, transitioning from a unicellular lifestyle to a coordinated multicellular entity, remains a fascinating question. Key events in this transition involved the emergence of processes related to cell adhesion, cell–cell communication and gene regulation. To understand how these capacities evolved, we need to reconstruct the features of both the last common multicellular ancestor of animals and the last unicellular ancestor of animals. In this review, we summarize recent advances in the characterization of these ancestors, inferred by comparative genomic analyses between the earliest branching animals and those radiating later, and between animals and their closest unicellular relatives. We also provide an updated hypothesis regarding the transition to animal multicellularity, which was likely gradual and involved the use of gene regulatory mechanisms in the emergence of early developmental and morphogenetic plans. Finally, we discuss some new avenues of research that will complement these studies in the coming years.

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Section: Phylogenetic Framework Of Animals and Their Unicellular Relativesmentioning

confidence: 99%

Section: Reconstruction Of the Biological Features Of The Last Unicellular Ancestor Of Animals And Last Common Ancestor Of Animals 221 Pomentioning

confidence: 99%

The origin of animals: an ancestral reconstruction of the unicellular-to-multicellular transition

et al. 2021

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“…In an initial bioinformatic survey, we noticed that nesfatin and phoenixin have a broad phyletic distribution, suggesting that these may be the oldest neuropeptides found so far. To analyse this in more detail, we searched the transcriptome and genome sequences of 45 metazoan species (Supplementary Table 1), two choanoflagellates, one filasterean, and Tunicaraptor unikontum, a predatory flagellate belonging to a newly identified animal-related lineage (Tikhonenkov, et al 2020). By sequence-similarity searches, multiple sequence alignments and gene-structure analyses, we identified homologs of the precursors of phoenixin (SMIM20) and nesfatin-1 (NUCB) across major groups of metazoans including Porifera, Ctenophora, Cnidaria, and in most of the bilaterian species analyzed.…”

Section: Phoenixin and Nesfatin-1 Precursors Were Already Present In The Last Common Ancestor Of Metazoa And Choanoflagellatesmentioning

confidence: 99%

Pre-metazoan origin of neuropeptide signalling

Yáñez-Guerra

Thiel

Jékely

2021

Preprint

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Neuropeptides are a diverse class of signalling molecules in metazoans. They occur in all animals with a nervous system and also in neuron-less placozoans. However, their origin has remained unclear because no neuropeptide shows deep homology across lineages and none have been found in sponges. Here, we identify two neuropeptide precursors, phoenixin and nesfatin, with broad evolutionary conservation. By database searches, sequence alignments and gene-structure comparisons we show that both precursors are present in bilaterians, cnidarians, ctenophores and sponges. We also found phoenixin and a secreted nesfatin precursor homolog in the choanoflagellate Salpingoeca rosetta. Phoenixin in particular, is highly conserved, including its cleavage sites, suggesting that prohormone processing occurs also in choanoflagellates. In addition, based on phyletic patterns and negative pharmacological assays we question the originally proposed GPR-173 (SREB3) as a phoenixin receptor. Our findings indicate that signalling by secreted neuropeptide homologs has pre-metazoan origins and thus evolved before neurons.

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“…( B ) Presence or absence of key Pfam domains analyzed in this study are represented in columns and color-coded according to genome or transcriptome data source (indicated in the Domain presence/absence key). The phylogenetic relationships of selected taxa are based on several recent phylogenomic studies ( Torruella et al 2015 ; Grau-Bové et al 2017 ; Hehenberger et al 2017 ; Tikhonenkov et al 2020 ; Urrutia et al 2021 ). Taxa are color-coded according to the Taxonomic Group key.…”

mentioning

confidence: 99%

“…To resolve these questions, we performed a taxonomically broad survey of genomic and transcriptomic sequence data representing all major eukaryotic supergroups, including newly sequenced protistan lineages within Holozoa ( Grau-Bové et al 2017 ; Hehenberger et al 2017 ; Tikhonenkov et al 2020 ; Urrutia et al 2021 ). We surveyed data from 180 species for key Rel homology DNA-binding and dimerization domain-containing proteins, examined their domain architecture, and constructed phylogenies of the proteins identified.…”

mentioning

confidence: 99%

Rel/NF-κB Transcription Factors Emerged at the Onset of Opisthokonts

Leger

Ros-Rocher

Najle

et al. 2022

Genome Biology and Evolution

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The Rel/NF-κB transcription factor family has myriad roles in immunity, development, and differentiation in animals, and was considered a key innovation for animal multicellularity. Rel homology domain-containing proteins were previously hypothesized to have originated in a last common ancestor of animals and some of their closest unicellular relatives. However, key taxa were missing from previous analyses, necessitating a systematic investigation into the distribution and evolution of these proteins. Here, we address this knowledge gap by surveying taxonomically broad data from eukaryotes, with a special emphasis on lineages closely related to animals. We report an earlier origin for Rel/NF-κB proteins than previously described, in the last common ancestor of animals and fungi, and show that even in the sister group to fungi, these proteins contain elements that in animals are necessary for the subcellular regulation of Rel/NF-κB.

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New Lineage of Microbial Predators Adds Complexity to Reconstructing the Evolutionary Origin of Animals

Cited by 38 publications

References 77 publications

The origin of animals: an ancestral reconstruction of the unicellular-to-multicellular transition

The origin of animals: an ancestral reconstruction of the unicellular-to-multicellular transition

Pre-metazoan origin of neuropeptide signalling

Rel/NF-κB Transcription Factors Emerged at the Onset of Opisthokonts

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