Animals have expanded the evolutionary legacy of unicellular ancestors in blood cells
Abstract
Blood cells are common and unique to animals, enabling them to address critical challenges of defense and transport. Thus, their evolution represents a defining innovation in metazoan multicellular life. However, their evolutionary trajectory about how blood cells emerged and diversified throughout animal history remains unclear. Here, we present a combination of bioinformatics and functional data that demonstrate that the metazoan blood cell program most likely originated through the repurposing of an ancestral premetazoan toolkit governed by Fos . This primordial program established the macrophage-like initial blood cells at the metazoan root. Then, the first lineage bifurcation at the origin of Bilateria drove the emergence of a specialized mast/killer lineage, characterized by acquisition of granular proteases for antiparasitic defense. Subsequent deuterostome/vertebrate innovations branched T/NK and erythrocyte/thrombocyte lineages from mast cells while B cells derived from macrophages. Our data also show that a prototypic thymus formed at the gill edges of a chordate ancestor. In line with the evolutionary history, the modern hematopoietic pathway shows a vestige of the phylogeny; differentiation potentials of phylogenetically old cell lineages expressing Fos such as macrophages and mast cells are widely retained, and ancient HSCs with limited lineage potentials have been inherited as origo-lineage progenitors. Our framework provides the history of blood cells showing an adaptive innovation built upon ancient unicellular foundations.
Article Details
Journal Info
Proceedings of the National Academy of Sciences
National Academy of Sciences
Authors (18)
Yosuke Nagahata
Laboratory of Immunology, Institute for Life and Medical Sciences, Kyoto University
Yuji Nishimura
Laboratory of Immunology, Institute for Life and Medical Sciences, Kyoto University
Ryota Kaitani
Laboratory of Immunology, Institute for Life and Medical Sciences, Kyoto University
Jason Cheok Kuan Leong
Research Center for Integrative Evolutionary Science, The Graduate University for Advanced Studies (SOKENDAI)
Izumi Oda-Ishii
Department of Zoology, Graduate School of Science, Kyoto University
Hisanori Kohtsuka
Misaki Marine Biological Station, School of Science, The University of Tokyo
Shinya Abe
Laboratory of Immune Regulation, Institute for Life and Medical Sciences, Kyoto University
Tasuku Ishida
Department of Zoology, Graduate School of Science, Kyoto University
Marina Carmona-Rivas
Department of Complexity of Life, Institut de Biologia Evolutiva (Consejo Superior de Investigaciones Científicas-Universitat Pompeu Fabra)
Sebastian R. Najle
Elena Casacuberta
Department of Complexity of Life, Institut de Biologia Evolutiva (Consejo Superior de Investigaciones Científicas-Universitat Pompeu Fabra)
Koichi Ikuta
Laboratory of Immune Regulation, Institute for Life and Medical Sciences, Kyoto University
Toru Miura
Misaki Marine Biological Station, School of Science, The University of Tokyo
Michio Ogasawara
Department of Biology, Graduate School of Science, Chiba University
Naoki Irie
Research Center for Integrative Evolutionary Science, The Graduate University for Advanced Studies (SOKENDAI)
Yutaka Satou
Department of Zoology, Graduate School of Science, Kyoto University
Iñaki Ruiz-Trillo
Hiroshi Kawamoto
Laboratory of Immunology, Institute for Life and Medical Sciences, Kyoto University