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

26 Pages Posted: 10 Jun 2020 Publication Status: Published

See all articles by Denis V. Tikhonenkov

Denis V. Tikhonenkov

Russian Academy of Sciences (RAS) - Papanin Institute for Biology of Inland Waters

Kirill V. Mikhailov

Moscow State University - Belozersky Institute for Physico-Chemical Biology

Elisabeth Hehenberger

GEOMAR Helmholtz Centre for Ocean Research Kiel - Ocean EcoSystems Biology Unit

Sergei A. Karpov

Russian Academy of Sciences (RAS) - Zoological Institute

Kristina I. Prokina

Russian Academy of Sciences (RAS) - Papanin Institute for Biology of Inland Waters

Anton S. Esaulov

Penza State University (PSU) - Department of Zoology and Ecology

Olga I. Belyakova

Penza State University (PSU) - Department of Zoology and Ecology

Yuri A. Mazei

Moscow State University - Department of General Ecology and Hydrobiology

Alexander P. Mylnikov

affiliation not provided to SSRN (deceased)

Vladimir V. Aleoshin

Moscow State University - Belozersky Institute for Physico-Chemical Biology

Patrick J. Keeling

University of British Columbia (UBC) - Department of Botany

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Abstract

The origin of animals is one of the most intensely studied evolutionary events, and our understanding of this transition was greatly advanced by analyses of unicellular protist relatives of animals, which have shown many “animal-specific” genes actually arose in protistan ancestors long before the emergence of animals. These genes have sometimes complex distributions and the protists have diverse lifestyles, so understanding their evolutionary significance requires both a robust phylogeny of animal relatives, and a detailed understanding of their biology. But discoveries of new animal-related lineages are rare and biased to bacteriovores and parasites. Here, we characterize the morphology, life cycle and transcriptome content of a new animal-related lineage, represented by the predatory flagellate, Tunicaraptor unikontum. Although it survives by preying on other eukaryotes, Tunicaraptor is an extremely small (3-5 μm) and morphologically simple cell; closely resembling some fungal zoospores. The Tunicaraptor transcriptome encodes a full complement of flagellar genes, which are only common to predatory animal relatives and missing in microbial parasites and grazers. Tunicaraptor also encodes several major classes of animal cell adhesion molecules and transcription factors and proteins involved in neurodevelopment that have not been found in other animal-related lineages. Phylogenomics including Tunicaraptor challenges the existing framework used to reconstruct the evolution of “animal specific” genes, and emphasizes that the diversity of animal-related lineages may be better understood only once the smaller, more inconspicuous animal-related lineages are better studied.

Keywords: Holozoa, phylogenomics, transcription factor, cell adhesion, Tunicaraptor, Protists, origin of animals

Suggested Citation

Tikhonenkov, Denis V. and Mikhailov, Kirill V. and Hehenberger, Elisabeth and Karpov, Sergei A. and Prokina, Kristina I. and Esaulov, Anton S. and Belyakova, Olga I. and Mazei, Yuri A. and Mylnikov, Alexander P. and Aleoshin, Vladimir V. and Keeling, Patrick J., New Lineage of Microbial Predators Adds Complexity to Reconstructing the Evolutionary Origin of Animals. Available at SSRN: https://ssrn.com/abstract=3606769 or http://dx.doi.org/10.2139/ssrn.3606769
This version of the paper has not been formally peer reviewed.

Denis V. Tikhonenkov (Contact Author)

Russian Academy of Sciences (RAS) - Papanin Institute for Biology of Inland Waters ( email )

Russia

Kirill V. Mikhailov

Moscow State University - Belozersky Institute for Physico-Chemical Biology ( email )

Russia

Elisabeth Hehenberger

GEOMAR Helmholtz Centre for Ocean Research Kiel - Ocean EcoSystems Biology Unit ( email )

Wischhofstrasse 1-3
Kiel, 24148
Germany

Sergei A. Karpov

Russian Academy of Sciences (RAS) - Zoological Institute ( email )

Russia

Kristina I. Prokina

Russian Academy of Sciences (RAS) - Papanin Institute for Biology of Inland Waters ( email )

Russia

Anton S. Esaulov

Penza State University (PSU) - Department of Zoology and Ecology ( email )

Krasnaya, 40
Penza, 440026
Russia

Olga I. Belyakova

Penza State University (PSU) - Department of Zoology and Ecology ( email )

Krasnaya, 40
Penza, 440026
Russia

Yuri A. Mazei

Moscow State University - Department of General Ecology and Hydrobiology ( email )

GSP-2, Leninskie Gory
Moscow, 119992
Russia

Alexander P. Mylnikov

affiliation not provided to SSRN (deceased)

Vladimir V. Aleoshin

Moscow State University - Belozersky Institute for Physico-Chemical Biology ( email )

Russia

Patrick J. Keeling

University of British Columbia (UBC) - Department of Botany ( email )

Canada

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