Solène Song1,2, Viktor Starunov3, Xavier Bailly4, Christine Ruta5, Pierre Kerner1, Annemiek J M Cornelissen2, Guillaume Balavoine6. 1. Institut Jacques Monod, Université de Paris / CNRS, UMR7592, Paris, France. 2. Laboratoire Matière et Systèmes Complexes, Université de Paris / CNRS, UMR7057, Paris, France. 3. Laboratory of Evolutionary Morphology, Zoological Institute, Russian Academy of Sciences, Universitetskaja nab. 1, 199034, Saint Petersburg, Russia. 4. Laboratoire des Modèles Marins Multicellulaires, Station Biologique de Roscoff, Sorbonne Université / CNRS, FR2424, Roscoff, France. 5. Laboratory of Integrative Biology of Marine Organisms, Institute of Biology, Federal University of Rio de Janeiro, Rio de Janeiro, RJ, Brazil. 6. Institut Jacques Monod, Université de Paris / CNRS, UMR7592, Paris, France. guillaume.balavoine@ijm.fr.
Abstract
BACKGROUND: How vascular systems and their respiratory pigments evolved is still debated. While many animals present a vascular system, hemoglobin exists as a blood pigment only in a few groups (vertebrates, annelids, a few arthropod and mollusk species). Hemoglobins are formed of globin sub-units, belonging to multigene families, in various multimeric assemblages. It was so far unclear whether hemoglobin families from different bilaterian groups had a common origin. RESULTS: To unravel globin evolution in bilaterians, we studied the marine annelid Platynereis dumerilii, a species with a slow evolving genome. Platynereis exhibits a closed vascular system filled with extracellular hemoglobin. Platynereis genome and transcriptomes reveal a family of 19 globins, nine of which are predicted to be extracellular. Extracellular globins are produced by specialized cells lining the vessels of the segmental appendages of the worm, serving as gills, and thus likely participate in the assembly of a previously characterized annelid-specific giant hemoglobin. Extracellular globin mRNAs are absent in smaller juveniles, accumulate considerably in growing and more active worms and peak in swarming adults, as the need for O2 culminates. Next, we conducted a metazoan-wide phylogenetic analysis of globins using data from complete genomes. We establish that five globin genes (stem globins) were present in the last common ancestor of bilaterians. Based on these results, we propose a new nomenclature of globins, with five clades. All five ancestral stem-globin clades are retained in some spiralians, while some clades disappeared early in deuterostome and ecdysozoan evolution. All known bilaterian blood globin families are grouped in a single clade (clade I) together with intracellular globins of bilaterians devoid of red blood. CONCLUSIONS: We uncover a complex "pre-blood" evolution of globins, with an early gene radiation in ancestral bilaterians. Circulating hemoglobins in various bilaterian groups evolved convergently, presumably in correlation with animal size and activity. However, all hemoglobins derive from a clade I globin, or cytoglobin, probably involved in intracellular O2 transit and regulation. The annelid Platynereis is remarkable in having a large family of extracellular blood globins, while retaining all clades of ancestral bilaterian globins.
BACKGROUND: How vascular systems and their respiratory pigments evolved is still debated. While many animals present a vascular system, hemoglobin exists as a blood pigment only in a few groups (vertebrates, annelids, a few arthropod and mollusk species). Hemoglobins are formed of globin sub-units, belonging to multigene families, in various multimeric assemblages. It was so far unclear whether hemoglobin families from different bilaterian groups had a common origin. RESULTS: To unravel globin evolution in bilaterians, we studied the marine annelid Platynereis dumerilii, a species with a slow evolving genome. Platynereis exhibits a closed vascular system filled with extracellular hemoglobin. Platynereis genome and transcriptomes reveal a family of 19 globins, nine of which are predicted to be extracellular. Extracellular globins are produced by specialized cells lining the vessels of the segmental appendages of the worm, serving as gills, and thus likely participate in the assembly of a previously characterized annelid-specific giant hemoglobin. Extracellular globin mRNAs are absent in smaller juveniles, accumulate considerably in growing and more active worms and peak in swarming adults, as the need for O2 culminates. Next, we conducted a metazoan-wide phylogenetic analysis of globins using data from complete genomes. We establish that five globin genes (stem globins) were present in the last common ancestor of bilaterians. Based on these results, we propose a new nomenclature of globins, with five clades. All five ancestral stem-globin clades are retained in some spiralians, while some clades disappeared early in deuterostome and ecdysozoan evolution. All known bilaterian blood globin families are grouped in a single clade (clade I) together with intracellular globins of bilaterians devoid of red blood. CONCLUSIONS: We uncover a complex "pre-blood" evolution of globins, with an early gene radiation in ancestral bilaterians. Circulating hemoglobins in various bilaterian groups evolved convergently, presumably in correlation with animal size and activity. However, all hemoglobins derive from a clade I globin, or cytoglobin, probably involved in intracellular O2 transit and regulation. The annelid Platynereis is remarkable in having a large family of extracellular blood globins, while retaining all clades of ancestral bilaterian globins.
Authors: Federico G Hoffmann; Juan C Opazo; David Hoogewijs; Thomas Hankeln; Bettina Ebner; Serge N Vinogradov; Xavier Bailly; Jay F Storz Journal: Mol Biol Evol Date: 2012-01-24 Impact factor: 16.240
Authors: Flávia A Belato; Christopher J Coates; Kenneth M Halanych; Roy E Weber; Elisa M Costa-Paiva Journal: Genome Biol Evol Date: 2020-10-01 Impact factor: 3.416
Authors: Ana B Christensen; Joseph L Herman; Maurice R Elphick; Kord M Kober; Daniel Janies; Gregorio Linchangco; Dean C Semmens; Xavier Bailly; Serge N Vinogradov; David Hoogewijs Journal: PLoS One Date: 2015-08-06 Impact factor: 3.240
Authors: Federico G Hoffmann; Jay F Storz; Shigehiro Kuraku; Michael W Vandewege; Juan C Opazo Journal: Genome Biol Evol Date: 2021-10-01 Impact factor: 3.416