Direct Evidence That Extracellular Giant Hemoglobin is Produced in Chloragogen Tissues in a Beard Worm, Oligobrachia mashikoi (Frenulata, Siboglinidae, Annelida)

Nakahama, Shigeyuki; Nakagawa, Taro; Kanemori, Masaaki; Fukumori, Yoshihiro; Sasayama, Yuichi

doi:10.2108/zsj.25.1247

“…These findings confirm the involvement of the mesodermal trophosome in hemoglobin metabolism and suggest that this organ is the site hematopoiesis. In the frenulate Oligobrachia mashikoi , the visceral mesoderm also strongly expresses globin subunits based on in situ hybridization and semiquantitative RT–PCR ( Nakahama et al 2008 ), but in this siboglinid, the visceral mesoderm is organized as simple peritoneum surrounding the endodermal trophosome ( Southward 1993 ).…”

Section: Resultsmentioning

confidence: 99%

Novel Insights on Obligate Symbiont Lifestyle and Adaptation to Chemosynthetic Environment as Revealed by the Giant Tubeworm Genome

Oliveira

¹

,

Mitchell

²

,

Girguis

³

et al. 2021

Molecular Biology and Evolution

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The mutualism between the giant tubeworm Riftia pachyptila and its endosymbiont Candidatus Endoriftia persephone has been extensively researched over the past 40 years. However, the lack of the host whole genome information has impeded the full comprehension of the genotype/phenotype interface in Riftia. Here we described the high-quality draft genome of Riftia, its complete mitogenome, and tissue-specific transcriptomic data. The Riftia genome presents signs of reductive evolution, with gene family contractions exceeding expansions. Expanded gene families are related to sulphur metabolism, detoxification, anti-oxidative stress, oxygen transport, immune system, and lysosomal digestion, reflecting evolutionary adaptations to the vent environment and endosymbiosis. Despite the derived body plan, the developmental gene repertoire in the gutless tubeworm is extremely conserved with the presence of a near intact and complete Hox cluster. Gene expression analyses establishes that the trophosome is a multi-functional organ marked by intracellular digestion of endosymbionts, storage of excretory products and haematopoietic functions. Overall, the plume and gonad tissues both in contact to the environment harbour highly expressed genes involved with cell cycle, programmed cell death, and immunity indicating a high cell turnover and defence mechanisms against pathogens. We posit that the innate immune system plays a more prominent role into the establishment of the symbiosis during the infection in the larval stage, rather than maintaining the symbiostasis in the trophosome. This genome bridges four decades of physiological research in Riftia, whilst simultaneously provides new insights into the development, whole organism functions and evolution in the giant tubeworm.

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“…HPC with very similar cytological properties have been described in other annelid species. They have been called perivasal cells because of their position around the lumen of vessels or extravasal cells, when they are located in the mesodermal peritoneum covering the gut in earthworms [56], siboglinids [57] or Arenicola [58]. In some sedentarian annelids such as Amphitrite [59], a specialized organ, the heart-body, produces the hemoglobins.…”

Section: The Hemoglobin-producing Cells: a Specialized Type Of Blood-mentioning

confidence: 99%

Globins in the marine annelid Platynereis dumerilii shed new light on hemoglobin evolution in bilaterians

Song

¹

,

Starunov

²

,

Bailly

³

et al. 2020

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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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“…These findings confirm the involvement of the mesodermal trophosome in haemoglobin metabolism and suggests that this organ is the site haematopoiesis. In the frenulate Oligobrachia mashikoi, the visceral mesoderm also strongly expresses globin subunits based on in-situ hybridisation and semi-quantitative RT-PCR (Nakahama et al 2008), but in this siboglinid the visceral mesoderm is organized as simple peritoneum surrounding the endodermal trophosome (Southward 1993).…”

Section: Substrate Transport For Energy Conservation and Biosynthesis Is Supported By Lineagespecific Adaptations And Parallel Evolutionamentioning

confidence: 99%

Novel insights on obligate symbiont lifestyle and adaptation to chemosynthetic environment as revealed by the giant tubeworm genome

Oliveira

¹

,

Mitchell

²

,

Girguis

³

et al. 2021

Preprint

0

View full text Add to dashboard Cite

The mutualism between the giant tubeworm Riftia pachyptila and its endosymbiont Candidatus Endoriftia persephone has been extensively researched over the past 40 years. However, the lack of the host whole genome information has impeded the full comprehension of the genotype/phenotype interface in Riftia. Here we described the high-quality draft genome of Riftia, its complete mitogenome, and tissue-specific transcriptomic data. The Riftia genome presents signs of reductive evolution, with gene family contractions exceeding expansions. Expanded gene families are related to sulphur metabolism, detoxification, anti-oxidative stress, oxygen transport, immune system, and lysosomal digestion, reflecting evolutionary adaptations to the vent environment and endosymbiosis. Despite the derived body plan, the developmental gene repertoire in the gutless tubeworm is extremely conserved with the presence of a near intact and complete Hox cluster. Gene expression analyses establishes that the trophosome is a multi-functional organ marked by intracellular digestion of endosymbionts, storage of excretory products and haematopoietic functions. Overall, the plume and gonad tissues both in contact to the environment harbour highly expressed genes involved with cell cycle, programmed cell death, and immunity indicating a high cell turnover and defence mechanisms against pathogens. We posit that the innate immune system plays a more prominent role into the establishment of the symbiosis during the infection in the larval stage, rather than maintaining the symbiostasis in the trophosome. This genome bridges four decades of physiological research in Riftia, whilst simultaneously provides new insights into the development, whole organism functions and evolution in the giant tubeworm.

show abstract

Direct Evidence That Extracellular Giant Hemoglobin is Produced in Chloragogen Tissues in a Beard Worm, Oligobrachia mashikoi (Frenulata, Siboglinidae, Annelida)

Cited by 4 publications

References 19 publications

Novel Insights on Obligate Symbiont Lifestyle and Adaptation to Chemosynthetic Environment as Revealed by the Giant Tubeworm Genome

Novel Insights on Obligate Symbiont Lifestyle and Adaptation to Chemosynthetic Environment as Revealed by the Giant Tubeworm Genome

Globins in the marine annelid Platynereis dumerilii shed new light on hemoglobin evolution in bilaterians

Novel insights on obligate symbiont lifestyle and adaptation to chemosynthetic environment as revealed by the giant tubeworm genome

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