Globins in the marine annelid Platynereis dumerilii shed new light on hemoglobin evolution in bilaterians
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...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2020-12-01
|
| Series: | BMC Evolutionary Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12862-020-01714-4 |
| _version_ | 1818359168586743808 |
|---|---|
| author | Solène Song Viktor Starunov Xavier Bailly Christine Ruta Pierre Kerner Annemiek J. M. Cornelissen Guillaume Balavoine |
| author_facet | Solène Song Viktor Starunov Xavier Bailly Christine Ruta Pierre Kerner Annemiek J. M. Cornelissen Guillaume Balavoine |
| author_sort | Solène Song |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-13T20:40:37Z |
| format | Article |
| id | doaj.art-d5e6fb6d3ac84b848b1d748ef926eb0a |
| institution | Directory Open Access Journal |
| issn | 1471-2148 |
| language | English |
| last_indexed | 2024-12-13T20:40:37Z |
| publishDate | 2020-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Evolutionary Biology |
| spelling | doaj.art-d5e6fb6d3ac84b848b1d748ef926eb0a2022-12-21T23:32:09ZengBMCBMC Evolutionary Biology1471-21482020-12-0120112310.1186/s12862-020-01714-4Globins in the marine annelid Platynereis dumerilii shed new light on hemoglobin evolution in bilateriansSolène Song0Viktor Starunov1Xavier Bailly2Christine Ruta3Pierre Kerner4Annemiek J. M. Cornelissen5Guillaume Balavoine6Institut Jacques Monod, Université de Paris / CNRS, UMR7592Laboratory of Evolutionary Morphology, Zoological Institute, Russian Academy of SciencesLaboratoire des Modèles Marins Multicellulaires, Station Biologique de Roscoff, Sorbonne Université / CNRS, FR2424Laboratory of Integrative Biology of Marine Organisms, Institute of Biology, Federal University of Rio de JaneiroInstitut Jacques Monod, Université de Paris / CNRS, UMR7592Laboratoire Matière et Systèmes Complexes, Université de Paris / CNRS, UMR7057Institut Jacques Monod, Université de Paris / CNRS, UMR7592Abstract 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.https://doi.org/10.1186/s12862-020-01714-4GlobinMetazoanBilaterianAnnelidConvergent evolutionBlood |
| spellingShingle | Solène Song Viktor Starunov Xavier Bailly Christine Ruta Pierre Kerner Annemiek J. M. Cornelissen Guillaume Balavoine Globins in the marine annelid Platynereis dumerilii shed new light on hemoglobin evolution in bilaterians BMC Evolutionary Biology Globin Metazoan Bilaterian Annelid Convergent evolution Blood |
| title | Globins in the marine annelid Platynereis dumerilii shed new light on hemoglobin evolution in bilaterians |
| title_full | Globins in the marine annelid Platynereis dumerilii shed new light on hemoglobin evolution in bilaterians |
| title_fullStr | Globins in the marine annelid Platynereis dumerilii shed new light on hemoglobin evolution in bilaterians |
| title_full_unstemmed | Globins in the marine annelid Platynereis dumerilii shed new light on hemoglobin evolution in bilaterians |
| title_short | Globins in the marine annelid Platynereis dumerilii shed new light on hemoglobin evolution in bilaterians |
| title_sort | globins in the marine annelid platynereis dumerilii shed new light on hemoglobin evolution in bilaterians |
| topic | Globin Metazoan Bilaterian Annelid Convergent evolution Blood |
| url | https://doi.org/10.1186/s12862-020-01714-4 |
| work_keys_str_mv | AT solenesong globinsinthemarineannelidplatynereisdumeriliishednewlightonhemoglobinevolutioninbilaterians AT viktorstarunov globinsinthemarineannelidplatynereisdumeriliishednewlightonhemoglobinevolutioninbilaterians AT xavierbailly globinsinthemarineannelidplatynereisdumeriliishednewlightonhemoglobinevolutioninbilaterians AT christineruta globinsinthemarineannelidplatynereisdumeriliishednewlightonhemoglobinevolutioninbilaterians AT pierrekerner globinsinthemarineannelidplatynereisdumeriliishednewlightonhemoglobinevolutioninbilaterians AT annemiekjmcornelissen globinsinthemarineannelidplatynereisdumeriliishednewlightonhemoglobinevolutioninbilaterians AT guillaumebalavoine globinsinthemarineannelidplatynereisdumeriliishednewlightonhemoglobinevolutioninbilaterians |