海洋无脊椎动物钝鳃鳗的球蛋白为两栖动物血红蛋白的进化提供了新的线索。

IF 3.4 Q1 Agricultural and Biological Sciences
Solène Song, Viktor Starunov, Xavier Bailly, Christine Ruta, Pierre Kerner, Annemiek J M Cornelissen, Guillaume Balavoine
{"title":"海洋无脊椎动物钝鳃鳗的球蛋白为两栖动物血红蛋白的进化提供了新的线索。","authors":"Solène Song, Viktor Starunov, Xavier Bailly, Christine Ruta, Pierre Kerner, Annemiek J M Cornelissen, Guillaume Balavoine","doi":"10.1186/s12862-020-01714-4","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>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.</p><p><strong>Results: </strong>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 O<sub>2</sub> 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.</p><p><strong>Conclusions: </strong>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 O<sub>2</sub> 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.</p>","PeriodicalId":9111,"journal":{"name":"BMC Evolutionary Biology","volume":"20 1","pages":"165"},"PeriodicalIF":3.4000,"publicationDate":"2020-12-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7771090/pdf/","citationCount":"0","resultStr":"{\"title\":\"Globins in the marine annelid Platynereis dumerilii shed new light on hemoglobin evolution in bilaterians.\",\"authors\":\"Solène Song, Viktor Starunov, Xavier Bailly, Christine Ruta, Pierre Kerner, Annemiek J M Cornelissen, Guillaume Balavoine\",\"doi\":\"10.1186/s12862-020-01714-4\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><strong>Background: </strong>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.</p><p><strong>Results: </strong>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 O<sub>2</sub> 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.</p><p><strong>Conclusions: </strong>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 O<sub>2</sub> 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.</p>\",\"PeriodicalId\":9111,\"journal\":{\"name\":\"BMC Evolutionary Biology\",\"volume\":\"20 1\",\"pages\":\"165\"},\"PeriodicalIF\":3.4000,\"publicationDate\":\"2020-12-29\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7771090/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"BMC Evolutionary Biology\",\"FirstCategoryId\":\"1085\",\"ListUrlMain\":\"https://doi.org/10.1186/s12862-020-01714-4\",\"RegionNum\":0,\"RegionCategory\":null,\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"Agricultural and Biological Sciences\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"BMC Evolutionary Biology","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1186/s12862-020-01714-4","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"Agricultural and Biological Sciences","Score":null,"Total":0}
引用次数: 0

摘要

背景:血管系统及其呼吸色素是如何进化而来的,目前仍存在争议。虽然许多动物都有血管系统,但血红蛋白作为一种血色素只存在于少数类群中(脊椎动物、无脊椎动物、少数节肢动物和软体动物)。血红蛋白由属于多基因家族的球蛋白亚单位组成,具有不同的多聚体组合。迄今为止,人们还不清楚不同两栖类的血红蛋白家族是否有共同的起源:为了揭示双翼类动物的球蛋白进化过程,我们研究了基因组进化缓慢的海洋无脊椎类动物Platynereis dumerilii。Platynereis有一个充满细胞外血红蛋白的封闭血管系统。Platynereis 的基因组和转录组揭示了一个由 19 个球蛋白组成的家族,其中 9 个被预测为细胞外球蛋白。细胞外球蛋白是由蠕虫节肢附属器血管内壁的特化细胞产生的,起到鳃的作用,因此很可能参与了先前表征的环带动物特异性巨型血红蛋白的组装。细胞外球蛋白 mRNA 在较小的幼虫体内缺失,在生长和活跃的蠕虫体内大量积累,并在成虫对氧气的需求达到高潮时达到顶峰。接下来,我们利用完整基因组的数据,对整个后生动物的球蛋白进行了系统进化分析。我们确定,双翼类最后的共同祖先中有五个球蛋白基因(茎球蛋白)。基于这些结果,我们提出了一个新的球蛋白命名法,其中包括五个支系。所有五个祖先茎球蛋白支系都保留在一些旋毛虫类中,而一些支系则在去壳类和低等动物进化的早期就消失了。所有已知的双足类血球蛋白家族都被归入一个支系(支系I),同时还包括没有红血的双足类细胞内球蛋白:我们发现了球蛋白复杂的 "前血液 "进化过程,以及祖先双翼类的早期基因辐射。不同双叶类群的循环血红蛋白是趋同进化的,这可能与动物的体型和活动有关。然而,所有的血红蛋白都来源于 I 族球蛋白或细胞血红蛋白,可能参与细胞内氧气的转运和调节。有孔虫类动物 Platynereis 的显著特点是拥有一个庞大的细胞外血球蛋白家族,同时保留了所有两栖类祖先的球蛋白支系。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
Globins in the marine annelid Platynereis dumerilii shed new light on hemoglobin evolution in bilaterians.

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.

求助全文
通过发布文献求助,成功后即可免费获取论文全文。 去求助
来源期刊
BMC Evolutionary Biology
BMC Evolutionary Biology 生物-进化生物学
CiteScore
5.80
自引率
0.00%
发文量
0
审稿时长
6 months
期刊介绍: BMC Evolutionary Biology is an open access, peer-reviewed journal that considers articles on all aspects of molecular and non-molecular evolution of all organisms, as well as phylogenetics and palaeontology.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信