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Guillaume Balavoine - One of the best experts on this subject based on the ideXlab platform.
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globins in the marine annelid platynereis dumerilii shed new light on hemoglobin evolution in bilaterians
BMC Evolutionary Biology, 2020Co-Authors: Solene Song, Viktor V Starunov, Xavier Bailly, Christine Ruta, Pierre Kerner, Annemiek Jm Cornelissen, Guillaume BalavoineAbstract: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. 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. 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.
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Globins in the marine Annelid Platynereis dumerilii shed new light on hemoglobin evolution in Bilaterians
2020Co-Authors: Solene Song, Viktor V Starunov, Xavier Bailly, Christine Ruta, Annemiek Cornelissen, Pierre Kerner, Guillaume BalavoineAbstract: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.
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globins and hemogenic cells in the marine annelid platynereis dumerilii shed new light on blood evolution in bilaterians
bioRxiv, 2019Co-Authors: Solene Song, Viktor V Starunov, Xavier Bailly, Christine Ruta, Annemiek Cornelissen, Pierre Kerner, Guillaume BalavoineAbstract:How vascular systems and their Respiratory Pigments evolved is still debated. To unravel blood evolution in Bilaterians, we studied the marine Annelid Platynereis dumerilii. Platynereis exhibits a closed vascular system filled with extracellular hemoglobin. An exhaustive screen in Platynereis genome reveals a family of 17 globins. Seven extracellular globins are produced by specialized hemogenic cells lining the vessels of the segmental appendages of the worm, serving as gills. Extracellular globins are absent in juveniles then accumulate considerably as the worm size and activity increase, culminating in swarming adults. Phylogenetic analyses with deep screenings in complete genomes establish that five globin genes (stem globins) were present in the last common ancestor of Bilaterians. All known Bilaterian blood globins are derived convergently from a single presumably ubiquitously expressed, intracellular stem globin gene. All five globin types are retained in Platynereis, reinforcing this species status as a key slow evolving genome within Bilaterians.
Arnaud Tanguy - One of the best experts on this subject based on the ideXlab platform.
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Molecular identification of differentially regulated genes in the hydrothermal-vent species Bathymodiolus thermophilus and Paralvinella pandorae in response to temperature
BMC Genomics, 2009Co-Authors: Isabelle Boutet, Didier Jollivet, Bruce Shillito, Dario Moraga, Arnaud TanguyAbstract:Background Hydrothermal vents and cold seeps represent oases of life in the deep-sea environment, but are also characterized by challenging physical and chemical conditions. The effect of temperature fluctuations on vent organisms in their habitat has not been well explored, in particular at a molecular level, most gene expression studies being conducted on coastal marine species. In order to better understand the response of hydrothermal organisms to different temperature regimes, differentially expressed genes (obtained by a subtractive suppression hybridization approach) were identified in the mussel Bathymodiolus thermophilus and the annelid Paralvinella pandorae irlandei to characterize the physiological processes involved when animals are subjected to long term exposure (2 days) at two contrasting temperatures (10° versus 20°C), while maintained at in situ pressures. To avoid a potential effect of pressure, the experimental animals were initially thermally acclimated for 24 hours in a pressurized vessel. Results For each species, we produced two subtractive cDNA libraries (forward and reverse) from sets of deep-sea mussels and annelids exposed together to a thermal challenge under pressure. RNA extracted from the gills, adductor muscle, mantle and foot tissue were used for B. thermophilus . For the annelid model, whole animals (small individuals) were used. For each of the four libraries, we sequenced 200 clones, resulting in 78 and 83 unique sequences in mussels and annelids (about 20% of the sequencing effort), respectively, with only half of them corresponding to known genes. Real-time PCR was used to validate differentially expressed genes identified in the corresponding libraries. Strong expression variations have been observed for some specific genes such as the intracellular hemoglobin, the nidogen protein, and Rab7 in P. pandorae , and the SPARC protein, cyclophilin, foot protein and adhesive plaque protein in B. thermophilus . Conclusion Our results indicate that mussels and worms are not responding in the same way to temperature variations. While the results obtained for the mussel B. thermophilus seem to indicate a metabolic depression (strong decrease in the level of mRNA expression of numerous genes) when temperature increased, the annelid P. pandorae mainly displayed a strong regulation of the mRNA encoding subunits and linkers of Respiratory Pigments and some proteins involved in membrane structure. In both cases, these regulations seem to be partly due to a possible cellular oxidative stress induced by the simulated thermal environment (10°C to 20°C). This work will serve as a starting point for studying the transcriptomic response of hydrothermal mussels and annelids in future experiments in response to thermal stress at various conditions of duration and temperature challenge.
Solene Song - One of the best experts on this subject based on the ideXlab platform.
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globins in the marine annelid platynereis dumerilii shed new light on hemoglobin evolution in bilaterians
BMC Evolutionary Biology, 2020Co-Authors: Solene Song, Viktor V Starunov, Xavier Bailly, Christine Ruta, Pierre Kerner, Annemiek Jm Cornelissen, Guillaume BalavoineAbstract: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. 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. 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.
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Globins in the marine Annelid Platynereis dumerilii shed new light on hemoglobin evolution in Bilaterians
2020Co-Authors: Solene Song, Viktor V Starunov, Xavier Bailly, Christine Ruta, Annemiek Cornelissen, Pierre Kerner, Guillaume BalavoineAbstract: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.
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globins and hemogenic cells in the marine annelid platynereis dumerilii shed new light on blood evolution in bilaterians
bioRxiv, 2019Co-Authors: Solene Song, Viktor V Starunov, Xavier Bailly, Christine Ruta, Annemiek Cornelissen, Pierre Kerner, Guillaume BalavoineAbstract:How vascular systems and their Respiratory Pigments evolved is still debated. To unravel blood evolution in Bilaterians, we studied the marine Annelid Platynereis dumerilii. Platynereis exhibits a closed vascular system filled with extracellular hemoglobin. An exhaustive screen in Platynereis genome reveals a family of 17 globins. Seven extracellular globins are produced by specialized hemogenic cells lining the vessels of the segmental appendages of the worm, serving as gills. Extracellular globins are absent in juveniles then accumulate considerably as the worm size and activity increase, culminating in swarming adults. Phylogenetic analyses with deep screenings in complete genomes establish that five globin genes (stem globins) were present in the last common ancestor of Bilaterians. All known Bilaterian blood globins are derived convergently from a single presumably ubiquitously expressed, intracellular stem globin gene. All five globin types are retained in Platynereis, reinforcing this species status as a key slow evolving genome within Bilaterians.
Isabelle Boutet - One of the best experts on this subject based on the ideXlab platform.
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Molecular identification of differentially regulated genes in the hydrothermal-vent species Bathymodiolus thermophilus and Paralvinella pandorae in response to temperature
BMC Genomics, 2009Co-Authors: Isabelle Boutet, Didier Jollivet, Bruce Shillito, Dario Moraga, Arnaud TanguyAbstract:Background Hydrothermal vents and cold seeps represent oases of life in the deep-sea environment, but are also characterized by challenging physical and chemical conditions. The effect of temperature fluctuations on vent organisms in their habitat has not been well explored, in particular at a molecular level, most gene expression studies being conducted on coastal marine species. In order to better understand the response of hydrothermal organisms to different temperature regimes, differentially expressed genes (obtained by a subtractive suppression hybridization approach) were identified in the mussel Bathymodiolus thermophilus and the annelid Paralvinella pandorae irlandei to characterize the physiological processes involved when animals are subjected to long term exposure (2 days) at two contrasting temperatures (10° versus 20°C), while maintained at in situ pressures. To avoid a potential effect of pressure, the experimental animals were initially thermally acclimated for 24 hours in a pressurized vessel. Results For each species, we produced two subtractive cDNA libraries (forward and reverse) from sets of deep-sea mussels and annelids exposed together to a thermal challenge under pressure. RNA extracted from the gills, adductor muscle, mantle and foot tissue were used for B. thermophilus . For the annelid model, whole animals (small individuals) were used. For each of the four libraries, we sequenced 200 clones, resulting in 78 and 83 unique sequences in mussels and annelids (about 20% of the sequencing effort), respectively, with only half of them corresponding to known genes. Real-time PCR was used to validate differentially expressed genes identified in the corresponding libraries. Strong expression variations have been observed for some specific genes such as the intracellular hemoglobin, the nidogen protein, and Rab7 in P. pandorae , and the SPARC protein, cyclophilin, foot protein and adhesive plaque protein in B. thermophilus . Conclusion Our results indicate that mussels and worms are not responding in the same way to temperature variations. While the results obtained for the mussel B. thermophilus seem to indicate a metabolic depression (strong decrease in the level of mRNA expression of numerous genes) when temperature increased, the annelid P. pandorae mainly displayed a strong regulation of the mRNA encoding subunits and linkers of Respiratory Pigments and some proteins involved in membrane structure. In both cases, these regulations seem to be partly due to a possible cellular oxidative stress induced by the simulated thermal environment (10°C to 20°C). This work will serve as a starting point for studying the transcriptomic response of hydrothermal mussels and annelids in future experiments in response to thermal stress at various conditions of duration and temperature challenge.
Pierre Kerner - One of the best experts on this subject based on the ideXlab platform.
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globins in the marine annelid platynereis dumerilii shed new light on hemoglobin evolution in bilaterians
BMC Evolutionary Biology, 2020Co-Authors: Solene Song, Viktor V Starunov, Xavier Bailly, Christine Ruta, Pierre Kerner, Annemiek Jm Cornelissen, Guillaume BalavoineAbstract: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. 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. 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.
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Globins in the marine Annelid Platynereis dumerilii shed new light on hemoglobin evolution in Bilaterians
2020Co-Authors: Solene Song, Viktor V Starunov, Xavier Bailly, Christine Ruta, Annemiek Cornelissen, Pierre Kerner, Guillaume BalavoineAbstract: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.
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globins and hemogenic cells in the marine annelid platynereis dumerilii shed new light on blood evolution in bilaterians
bioRxiv, 2019Co-Authors: Solene Song, Viktor V Starunov, Xavier Bailly, Christine Ruta, Annemiek Cornelissen, Pierre Kerner, Guillaume BalavoineAbstract:How vascular systems and their Respiratory Pigments evolved is still debated. To unravel blood evolution in Bilaterians, we studied the marine Annelid Platynereis dumerilii. Platynereis exhibits a closed vascular system filled with extracellular hemoglobin. An exhaustive screen in Platynereis genome reveals a family of 17 globins. Seven extracellular globins are produced by specialized hemogenic cells lining the vessels of the segmental appendages of the worm, serving as gills. Extracellular globins are absent in juveniles then accumulate considerably as the worm size and activity increase, culminating in swarming adults. Phylogenetic analyses with deep screenings in complete genomes establish that five globin genes (stem globins) were present in the last common ancestor of Bilaterians. All known Bilaterian blood globins are derived convergently from a single presumably ubiquitously expressed, intracellular stem globin gene. All five globin types are retained in Platynereis, reinforcing this species status as a key slow evolving genome within Bilaterians.